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R E S E A R C H Open Access

Changes in the geographical distribution andabundance of the tick Ixodes ricinus during thepast 30 years in Sweden

Thomas GT Jaenson1*, David GE Jaenson1, Lars Eisen2, Erik Petersson3 and Elisabet Lindgren4

Abstract

Background: Ixodes ricinus is the main vector in Europe of human-pathogenic Lyme borreliosis (LB) spirochaetes,the tick-borne encephalitis virus (TBEV) and other pathogens of humans and domesticated mammals. The results of

a previous 1994 questionnaire, directed at people living in Central and North Sweden (Svealand and Norrland) andaiming to gather information about tick exposure for humans and domestic animals, suggested that Ixodes ricinusticks had become more widespread in Central Sweden and the southern part of North Sweden from the early1980s to the early 1990s. To investigate whether the expansion of the ticks northern geographical range and theincreasing abundance of ticks in Sweden were still occurring, in 2009 we performed a follow-up survey 16 yearsafter the initial study.

Methods: A questionnaire similar to the one used in the 1994 study was published in Swedish magazines aimedat dog owners, home owners, and hunters. The questionnaire was published together with a popular sciencearticle about the ticks biology and role as a pathogen vector in Sweden. The magazines were selected to getinformation from people familiar with ticks and who spend time in areas where ticks might be present.

Results: Analyses of data from both surveys revealed that during the near 30-year period from the early 1980s to2008, I. ricinus has expanded its distribution range northwards. In the early 1990s ticks were found in new areas

along the northern coastline of the Baltic Sea, while in the 2009 study, ticks were reported for the first time frommany locations in North Sweden. This included locations as far north as 66N and places in the interior part ofNorth Sweden. During this 16-year period the ticks range in Sweden was estimated to have increased by 9.9%.Most of the range expansion occurred in North Sweden (north of 60N) where the ticks coverage area doubledfrom 12.5% in the early 1990s to 26.8% in 2008. Moreover, according to the respondents, the abundance of tickshad increased markedly in LB- and TBE-endemic areas in South (Gtaland) and Central Sweden.

Conclusions: The results suggest that I. ricinus has expanded its range in North Sweden and has become distinctlymore abundant in Central and South Sweden during the last three decades. However, in the northern mountainregion I. ricinus is still absent. The increased abundance of the tick can be explained by two main factors: First, thehigh availability of large numbers of important tick maintenance hosts, i.e., cervids, particularly roe deer (Capreoluscapreolus) during the last three decades. Second, a warmer climate with milder winters and a prolonged growingseason that permits greater survival and proliferation over a larger geographical area of both the tick itself and

deer. High reproductive potential of roe deer, high tick infestation rate and the tendency of roe deer to dispersegreat distances may explain the range expansion of I. ricinus and particularly the appearance of new TBEV foci faraway from old TBEV-endemic localities. The geographical presence of LB in Sweden corresponds to the distributionof I. ricinus. Thus, LB is now an emerging disease risk in many parts of North Sweden. Unless countermeasures areundertaken to keep the deer populations, particularly C. capreolus and Dama dama, at the relatively low levels that

* Correspondence: [email protected] Entomology Unit, Department of Systematic Biology, EvolutionaryBiology Centre, Uppsala University, Norbyvgen 18d, SE-752 36 Uppsala,SwedenFull list of author information is available at the end of the article

Jaenson et al. Parasites & Vectors 2012, 5:8

http://www.parasitesandvectors.com/content/5/1/8

2012 Jaenson et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative CommonsAttribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction inany medium, provided the original work is properly cited.
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prevailed before the late 1970s - especially in and around urban areas where human population density is high -by e.g. reduced hunting of red fox (Vulpes vulpes) and lynx (Lynx lynx), the incidences of human LB and TBE areexpected to continue to be high or even to increase in Sweden in coming decades.

BackgroundThe annual incidences in Europe of tick-borne diseases,particularly Lyme borreliosis (LB) and tick-borne ence-phalitis (TBE), have been increasing since the 1980s [1,2].In Sweden, since 1988 every year except 1996 and 2010has been warmer or much warmer than the long-termaverage for 1961-1990. Furthermore, between 1880 and2009 the mean temperature in Sweden increased by 2C[3]. This is in line with an increasing green-house effect[4]. During the same time period mean global tempera-tures increased and further warming is predicted [5].This poses the question of whether or not there is acause-and-effect relationship so that a warmer climatedirectly and/or indirectly contributes to increased tickabundance and increased intensity or geographical rangeof enzootic pathogen transmission leading to greater riskfor human disease [6-9]. Biological phenomena or pro-cesses usually depend on many interacting factors. Insome European countries climate change may have hadonly a marginal effect on the recent increase in humanincidence of TBE; Instead, political and socio-economicalterations were presumably the main drivers causingincreased contact between humans and infective ticksthereby augmenting the incidence of human TBE [10,11].

Before the early 1980s the northern range limit of thepathogen-transmitting tick, I. ricinus, was considered tobe determined by the important biogeographical bound-ary called Limes Norrlandicus (LN), which runs throughCentral Sweden and separates the Nemoral zone to thesouth of the LN from the Boreal zone to the north [12].The first comprehensive mapping of the geographicaldistribution ofI. ricinus in Sweden was carried out in1992-94 [13]. Moreover, in 1994 a questionnaire studywas performed with the aim of exploring whether thenorthern limit of the tick had changed [14]. The newnorthern boundary for I. ricinus was shown to run

through Central Sweden and along coastal North Swe-den. During the same period the main host in Sweden foradults ofI. ricinus, the roe deer (Capreolus capreolus)rapidly increased its population size: In 1955 there wereabout 100 000 roe deer in Sweden. In 1985 the popula-tion numbered about 300 000 deer when it began toincrease more rapidly: in 1993-94 it was > 1 million deer[15,16]. Main reasons for this population explosionwere an epizootic of scabies (Sarcoptes scabiei) in the twomost important predators of roe deer, namely the red fox(Vulpes vulpes) and the lynx (Lynx lynx) [17,18] popula-tions from early 1970s to late 1980s, and a series of mild

winters during the early 1990s [16]. These factorsreduced mortality and promoted survival and reproduc-tion of roe deer. Both predator populations increasedduring the 1990s which, together with deer hunting,resulted in a decline of the roe deer population. The lastcensus in 2005 estimated the roe deer population in Swe-den to be about 375 000 deer [15,19] when more roedeer were shot than the total population numbered 50

years earl ier. Since 2005 the roe deer population hasdeclined further, especially during the two harsh winters,with deep snow cover, in 2009-10 and 2010-11 [15,19].

About 1,200 respondents, mainly from Central andNorth Sweden answered the short questionnaire that waspublished in the spring of 1994 in national free maga-zines for home owners, local newspapers and two majormagazines for dog owners [14]. The questionnaire asked,among other things, if ticks were present in the vicinityof the respondents residence during the previous two

years (1992-1993) and in the early 1980s. The results sug-gested that, during this 10-year period, I. ricinus hadspread to new localities north of its previous range; andacross most of its previous northern range ticks hadbecome more abundant. The answers to the question-naire also suggested that there was a boundary zone

across south-central Sweden where tick abundance chan-ged from high in the southern part to low in the northernpart of the zone [14]. In August-September 1994-96 thedensity of ticks was estimated by cloth-dragging at 57localities in the hypothetical boundary zone between 6010 and 60 55N. The results of that field study con-firmed that there was such a boundary zone; to the southof this zone host-seeking I. ricinus ticks could, in general,be found but not to the north of it except sparsely alongthe Baltic Sea coastline [14].

A similar picture has been documented in Central Eur-ope: In the mountainous regions of the Czech Republic,

I. ricinus is now present at higher altitudes than in the1980s [20,21]. This changed tick distribution is associatedwith increased temperatures at higher altitudes [21]. InDenmark, tick density was found to be related to roedeer density [22] and the drastic increase in tick abun-dance in Denmark from 1985 to the beginning of the1990s could be explained by increased temperatures anddeer density[23]. A survey throughout Great Britainindicated that the opinion of most people was that thereare more ticks today than in the past and that theseincreases in tick abundance coincided spatially withincreases in deer numbers [24]. A recent analysis of



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various data on ticks and tick-borne pathogens collectedover several decades in Norway indicated that I. ricinus isnow found further to the north and at higher altitudesthan a few decades ago [25].

Both the latitudinal changes in tick distribution andabundance in Sweden and the altitudinal changes in theCzech Republic have been found to be correlated withchanges in temperatures and number of degree-days perseason [7,20,26]. Since the 1990s changes in climate havecontinued [3,5] which may have further influenced therange and abundance ofI. ricinus in Sweden. In addition,previous studies have shown that the risk of contractingLB in Sweden coincides with the distribution and densityofI. ricinus [7,27-30]. In other words, changes in tick dis-tribution and density are likely to have increased the riskof human LB and are likely to lead to further changes inrisk areas for LB.

This study was a follow-up investigation 15 years afterthe first major national investigation of the distributionand abundance ofI. ricinus in Sweden took place. Ourmain aim was to investigate if there had been anychanges, since the 1994 study, in distribution and abun-dance ofI. ricinus in Central and North Sweden.

MethodsIn April-June 2009 a short questionnaire (Appendix 1),almost identical to the one used in 1994, was attached toa popular science article on ticks and tick-borne diseaseswhich was published in the free magazines Apoteket(The Pharmacy; available from May-August 2009 at allSwedish pharmacies) and Vi i Villa (We Home Owners;distributed to all Swedish home owners), as well as inmajor national journals for dog owners (Brukshunden;The Service Dog) and hunters (Svensk Jakt; SwedishHunting), in four local North-Swedish newspapers(Lnstidningen stersund, Norran, Norrbottenskuriren,Pitetidningen), and on a Swedish website http://www.blodsugare.se with information about ticks and tick-borne infections.

In the questionnaire of the 2009 study we asked forinformation about the occurrence of ticks within 1 km ofthe respondents residence. We pointed out that we were

particularly interested in answers from the northern andcentral regions of Sweden. If ticks were reported to bepresent, a follow-up question focused on approximatelyhow many were found on each family member and oneach one of the familys dog(s) and cat(s) in 2008. In theanalyses of these data, responses of many, several orsome rather than a numerical value were excludedfrom the calculations of median numbers of ticks ontick-infested hosts (with at least one tick found per hostduring the tick season). The numbers of uninfested hostswere recorded separate from the infested hosts to permitcalculations of percentages of hosts without any tick(s)

recorded on their bodies. We also asked if ticks were pre-sent in the same area in the beginning of the 1990s, andif the respondent considers ticks to have become more orless prevalent since that time period, or if no obviouschange in tick abundance had occurred. We specificallystated that we were equally interested in No answers asin Yes or No change answers. We also asked for ticks(removed from humans and domestic animals, includinginformation about date of collection, locality and hostspecies) to be sent for species identification to one of theauthors (TJ). The identification of these ticks is in pro-gress and will be presented in a separate publication.However, in Sweden nearly all (> 99%) ticks found onhumans, dogs, cats, horses, cattle, hares and deer are I.ricinus [13]. We therefore consider the data presented inthis paper to refer to I. ricinus. The word tick, whenused in this article, denotes I. ricinus.

In the Results section we use the term distant mem-ory answers to denote answers that indicate that therespondent tries to remember the tick situation > 10

years ago. The term actual, near-present tick situationis used to indicate that the respondent attempts toremember the tick situation 1-2 years ago.

Critique of the questionnaire-based method usedThe ideal way to detect changes in the geographic rangeand density ofI. ricinus would be to sample for ticks reg-ularly at many locations throughout the country, even atlocations where the tick is presently not known to occur.Such a tick monitoring programme would be exceedinglytime-consuming and expensive and, therefore, has notand is not carried out in Sweden. In the absence of sucha surveillance programme we consider that this investiga-tion, based on questionnaires, is an appropriate alterna-tive. However, we want to emphasize that some factorsreduce the reliability of the data collected. Positive resultsare likely to be reported more frequently than negativeones. Therefore, data may be biased towards locationswhere ticks were present, where ticks had increased inabundance or where they had recently become estab-lished [24]. People are nowadays likely to be much moreaware of what a tick looks like and more alert to detect

ticks compared to in the 1960s-70s, i.e., before Lyme bor-reliosis had been described. Also, people generallyremember more correctly something that happenedrecently compared to things that happened long ago.These phenomena presumably influenced the data.Furthermore, people interested in tick biology, personswho have contracted a tick-borne disease and peoplewho have many ticks in their garden, on their cats ordogs, etc. are more likely than others to answer the ques-tionnaire. In the questionnaire, we stated that we wereequally interested in receiving negative answers, i.e. noticks present, as positive answers. Thus, another



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potentially biasing factor is that people, particularly inNorth Sweden where ticks had rarely been observedbefore ca. 1990, who recently had discovered ticks neartheir homes were presumably more prone to respondmore readily to the questionnaire than people who hadnever observed any ticks near their homes.

Data analysesOnly questionnaires (N = 1,032) that provided accepta-ble, i.e. complete answers for both time periods (early1990s and 2008) were included in the analyses. Data ontick occurrence (presence/absence) in the differentregions were calculated using generalized linear methods[31], binomial distribution, i.e. logistic regression; regionbeing the class variable. The response variable beingnumber of adequately filled in questionnaire formsreporting ticks out of the total number of correctly filled

in questionnaires for each province (see Figure 1). If anoverall difference between regions was indicated we per-formed a post-hoc pair-wise test for the probability oftick presence. In this case we used a Wald c2. The Waldtest [32] is based on the idea that we accept the nullhypothesis when the observed is close to 0. The dis-tance between observed and 0 is the basis of construct-ing the test statistics. Typically the square of thedifference is compared to a c2-distribution [33].

The data for tick presence on man, dog or cat couldnot be analyzed with general linear methods. Instead anordinary ANOVA was performed, and the pair-wise com-parisons among regions were done using the t-test. Datafor other pair-wise comparisons, e.g. change in tick abun-dance before vs. after a certain time, exhibited a non-nor-mal distribution. In these cases, we used Wilcoxonsmatched-pair signed-ranks test. To test for differences inchange between regions or provinces the Kruskal-Wallistest was used. If an overall difference among regions orprovinces was found a non-parametric pair-wise compar-ison method was used (Dunns test). For most statisticalanalyses we used SAS 9.2 statistical software. However,Wilcoxons matched-pair signed-ranks test was calcu-lated by hand according to Siegel & Castellan [34] andthe non-parametric pair-wise comparisons (Dunns test)

were calculated according to Hollander & Wolfe [35].A computer program, written in PHP 5.4 beta 1 [36] was

used to measure the number of pixels (where one pixelcorresponds to 2.64 2.64 km) showing the estimatedranges ofI. ricinus in the early 1990s and 2008 (Figure 2).The area where the tick was present in the early 1990s(Figure 2, left, black area) is based on Figure 3 (left mapand Table 1) and a map with confirmed records ofI. rici-nus ticks identified in the laboratory (published in [13]).The map for 2008 (Figure 2, right, black) is based on the2009 questionnaire reports of tick presence shown inFigure 3 (right map) and Table 1. By subtracting the

number of pixels of the black area in the left map(Figure 2) from the number of pixels in black area of theright map (Figure 2) we obtained an estimate, expressed asa percentage, of how much the ticks range had changedfrom the early 1990s to 2008.

Data recorded in this study of 2009 was comparedwith data collected in 1994 covering the period from theearly 1980s to 1993 and published by Tlleklint andJaenson [14]. In the questionnaires of 1994 and 2009 weused the terms early 1980s and early 1990s, respec-tively. We estimated these terms to signify ~1983 and~1993, respectively. Thus, the first study period repre-sents the years ~1983-1993 = ~11 years and the secondperiod ~1993-2008 = ~16 years.

Names of the Swedish provinces (landskap) are abbre-viated to two capi ta l le tters in accordance with therecommendations of the Swedish Entomological Society

(Figure 1).

ResultsGeographical distribution and abundance of I. ricinusticksOut of the 1,121 completed questionnaires returned byrespondents to us, 1,032 questionnaires included com-plete answers for both time periods (early 1990s and2008) and thus were deemed acceptable for inclusion indata analyses. During the early 1990s ticks werereported to be present in the vicinity of the homes ofmost respondents living in South Sweden (i.e. the pro-

vinces SK, BL, L, GO, HA, VG, SM, G, BO; 67.0% ofreplies indicating tick presence) and Central Sweden(DS, VR, N, VS, S, UP; 68.6% of replies indicatingtick presence) (Table 1; Figure 3). By 2008, presence ofticks was reported even more commonly by respondentsin South Sweden (99.1%) and Central Sweden (99.7%)(Table 1, Figure 3). Thus, by 2008 ticks were apparentlypresent in practically all areas of South and CentralSweden. The data from North Sweden indicated dra-matic increases in tick presence from the early 1990s to2008. This included statistically significant increasesfrom 33.3 to 97.4% for the southern part of North Swe-den (DR, G, HS); from 14.8 to 90.2% in the central

part of North Sweden (ME, N, HR, J, VB); and from9.5 to 73.0% for the two northernmost provinces inNorth Sweden (NB, LP).

All Swedish tick records known to us were compiledduring 1992-94 and published in [13]. Data from ourfirst tick questionnaire study in 1994 were published in1998 [14]. Both investigations showed that I. ricinus waspresent in all North-Swedish provinces except Hrjeda-len (HR). A similar pattern, i.e., with presence recordsof I. ricinus from all Swedish provinces except HRremained when the data of the 2009 questionnnairestudy (this investigation) were analyzed. However, very



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recently - in August 2011 - we received on two separateoccasions a total of four adult blood-fed tick femalesremoved from two dogs treated at the District Veterin-ary Clinic at Hede, Hrjedalen. These ticks were

microscopically identified as I. ricinus and are now thefirst published finding of this species from Hrjedalen.The dogs had not been away from the province duringfour weeks prior to detection of the ticks.

Figure 1 Swedish provinces (landskap) and their abbreviations.



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The results referring to 2008 (Figure 3) differ from thesituation observed in the early 1990s in Central andNorth Sweden when ticks were, in general, only presentclose to the Baltic Sea Coast and only rarely encounteredin the interior areas (Figure 2, based on a map previouslypublished in Jaenson et al. [13]). This corroborates theimpression of the maps in Figure 3 that from the early1990s to 2008 the range of I. ricinus increased, particu-larly in North Sweden. Further to the south, ticks were

already present in most locations investigated in the early1990s (Figure 3 in [13]; Figure 2).

The estimated ranges ofI. ricinus in Sweden in the early1990s and 2008 are shown in Figure 2. Based on the num-ber of tick presence pixels in each of the two maps, calcu-lations revealed that the ticks distributional area inSweden increased by 9.9% from early 1990s (41.6%) to2008 (51.5%). Most of this range expansion occurred inNorth Sweden along the Baltic Sea coast. For North

Figure 2 Estimated ranges of I. ricinus in Sweden in the early 1990s (left map) and 2008 (right map).



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Sweden (north of 60N) the ticks range increased by14.3%, doubling from early 1990s (12.5%) to 2008 (26.8%).

Comparison of tick occurrence between the study of1994 and the present studyWe compared data on tick occurrence for the two periods,i.e., the early 1980s - 1993 (i.e., questionnaire data recordedin 1994 and published in [14]) versus the early 1990s -2008 (the present study of 2009). The % change in Table1 refers to the percentage of respondents that consideredticks to be present within 1 km from the respondentshome. Statistical analysis suggests that the increase in %change in the three northern regions combined during theearly 1990s - 2008 was greater than the % change duringthe early 1980s-1993 (Wald c2 = 16.32, p < 0001). In this

analysis we took into account that the first period (early1980s - 1993) is 11 years and the second period (early1990s - 2008) 16 years. There was no interaction between

region (Southern North, Central North, and NorthernNorth Sweden) and time period (Wald c2 = 0.6417, P =0.726). This suggests that the percentage increase was simi-lar in the three northern regions.

Change in tick distribution and abundance from early1990s to 2008The previous results refer to presence or absence ofticks within 1 km of the respondents home. In 2009 wealso asked if respondents considered tick numbers, i.e.,tick abundance to have changed between the early1990s and 2008. The next last column of Table 1 shows

Figure 3 Maps showing localities in Central and North Sweden where ticks ( I. ricinus) were reportedly present () or absent (o)according to the respondents to a national tick survey in 2009 . Left map refers to the early 1990s and right map to 2008.



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that in all regions, except the Baltic Islands, a significantproportion of the respondents considered that ticks hadbecome more common (i.e., more numerous) since theearly 1990s. The increased tick abundance was regardedas lower in the regions Baltic Islands and NorthernNorth Sweden compared to the other regions.

In South and Central Sweden, where ticks were reportedto have been present in 64.5-80% of the locations in theearly 1990s, nearly all (98.9-100.0%) respondents statedthat ticks now (2008) occur in the vicinity of theirhomes (Table 1). For North Sweden, there is a distinctincrease reported in a number of locations where ticks arecurrently (2008) present compared to 16 years earlier. Forexample, in Central North Sweden respondents statedticks to be present in 14.8% of locations in the early 1990scompared to 90.2% in 2008. For northernmost Sweden thecorresponding proportions were 9.5% in early 1990s and

73% in 2008 (Table 1). In general the respondents answersabout presence of ticks gave greater values in 2008 than in1994 (z = 1.761, p = 0.0392; Wilcoxons matched-pairsigned-rank test). The change in tick presence between1993 and 2008 differed between the regions (c2 = 12.22,p = 0.016, Kruskal-Wallis test). Dunns test for pair-wisecomparisons revealed that the % change in tick presencefrom early 1990s to 2008 was greatest in the three regionsof North Sweden and differed significantly from those ofthe Central and Southern regions (Table 1). During thesame period, there was no significant difference in %change among the regions of North Sweden (Table 1).Similarly, no significant difference was found in % changeamong the four southern regions (Central, West Coast,Baltic Islands and southernmost Sweden (Table 1).

The questionnaire results are affected by fading memorywith timeThe distant memory-based tick presence questionnairedata referring to the early 1990s to 2008 and collected inthe study of 2009 were compared to the estimates of tickpresence based on near-present memory for 1993 (studyof 1994) and 2008 (study of 2009). The estimated change,increase in this case, according to respondents distant(faded) memory was that tick presence increased on aver-

age 3.0 2.9 times for the whole of Sweden, but accordingto actual near-present memory the estimated changewas only 1.3 0.5 times (t = 2.64, d.f. = 23.39, p = 0.0145,Satterthwaites methods for unequal variance). Thus, theincrease was greater according to distant memory com-pared to near-present, actual estimates. This likelyreflects that the memory of the respondents becomes lessreliable with time.

Number of ticks per infested hostThe estimated median numbers of ticks collected by therespondents on themselves and on their dogs or cats

during the tick season of 2008 are shown for the differentregions in Table 2. The median numbers of ticks recordedper respondent ranged between 4 and 7 in South and Cen-tral Sweden but were significantly lower (1-2) in NorthSweden. For cats there is a tendency that tick numberswere greater in Central and South Sweden (20-30) than inNorth Sweden (2-11; Table 2). A similar tendency,although not statistically significant, was indicated by themedian numbers of ticks on dogs: 12.5-25 for South andCentral Sweden compared to 2-10 for North Sweden(Table 2). The proportion of uninfested hosts increasedfrom southern Sweden towards the north (Table 2). Thislikely reflects the lower tick abundance in the north.

DiscussionChange in tick range and tick abundanceThe results from both 1994 and 2008 surveys suggest

that the range ofI. ricinus increased markedly in Swedenduring the period from the early 1980s to 2008. Thisrange expansion appears quite distinct at the northernparts of the tick s range. Thus, I. ricinus now occurs inmany localities in the interior and northernmost regionsof Norrland in places where it was not present aboutthree decades ago, albeit at lower densities compared toSouth and Central Sweden and the southern part ofNorth Sweden. It should be noted that in contrast toSouth Sweden homesteads are to a greater extent locatedin the climatologically most suitable places which arealong the coast and rivers in inland river valleys, aroundlakes and other low-land areas as far as possible pro-tected from the cold northern climate. Therefore, therecords ofI. ricinus in Northern Sweden mainly refer tosuch clusters of respondents living in places with amilder climate, with a more southern vegetation andfauna than that of the surrounding boreal areas domi-nated by spruce and pine (taiga) forest.

Both questionnaire-based studies showed that therewas a significant increase in the proportion of respon-dents that considered that ticks are presently (referringto the previous years tick season) occurring near therespondents homes, compared to 11-16 years ago. Com-parison of the percentage increase in tick occurrence was

greater, i.e., significantly more rapid during the secondquestionnaire study period (1993-2008) than during thefirst period (1983-1993). The winters of 1988 to 1995were warm or exceptionally warm in Sweden [3]. Asmentioned, this corresponds to the period when, due tothe mild winters and a reduced fox population the num-ber of roe deer increased dramatically to reach more than1 million deer in 1994. The subsequent increase in foxand lynx numbers together with hunting began to reducethe roe deer population.

In view of the extended life cycle duration of I. ricinuswhich may be as long as 6 years in Northern Europe



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[37], there is a time lag of several years between a peakin the deer population and the resulting high I. ricinuspopulation [38]. Thus, it is inferred that the greater %change per year of tick occurrence during the second

study period (1993-2008) compared to that of the firstperiod (1983-1993) is due to two factors: First, the highavailability of large maintenance hosts, i.e. mainly roedeer, in particular during the late 1980s and early partof the 1990s should have been favourable especially forthe adult ticks to reproduce and thereby for the tickpopulation to increase. This conclusion is supported bydata recorded at the Danish Pest Infestation Laboratory(DPIL) [23]: The annual numbers of requests for infor-mation on I. ricinus - a proxy for tick abundance - toDPIL was fairly stable between 1965 to 1985, butdoubled during the late 1980s to reach a higher level inthe early 1990s. The perceived tick abundance corre-lated with estimates of annual deer abundance and tem-perature records [23].

Second, for most European meteorological stations temperature records the mean annual temperature showsa marked step-increase around 1989 and has thereafterbeen followed by consistently warm conditions [4,38].Such an increased warming, most of which occurredfrom January to early August [38] should both directlyand indirectly have favoured survival and reproduction ofboth roe deer and ticks [7]. Indirectly, climatic changescan significantly influence vegetation communities and

tick host populations. Recent studies have shown a closecorrespondence between the durations of the vegetationperiod and snow cover period and the distributional areafor I. ricinus in Sweden [7,39]. The tick is unlikely to

become established in an area where the snow cover per-iod is > 150 days/year and where the mean temperatureis < 5C for > 170 days. This suggests that a direct orindirect effect of the climate, i.e., temperatures within acertain range, determine the potential geographical distri-bution ofI. ricinus - given that precipitation and humid-ity are adequate.

Like many other vectors of zoonotic pathogens [40]I.ricinus is a host- and habitat-generalist with a very widehost range and has been recorded from many differentbiotopes. The survival and proliferation of such ectopara-sites are obviously dependent, in part, on the communityof host species which they infest [40]. In general, themain hosts of adult I. ricinus on the Swedish mainlandare cervids [13]. If, during a period of several years theclimate is above average favourable for these mamma-lian tick hosts, they would presumably expand theirpopulation sizes and ranges - on the assumption that dis-ease, predation and hunting pressure do not increase andthat other tick hosts do not change their impact on thetick population. A corollary would be that I. ricinus, inthe same area where the cervids occur, would most likelyincrease its geographical range and become more abun-dant. This is most likely what happened on the Swedish

Table 2 Median number (in bold) of ticks per tick-infested host, i.e., respondent ( Homo sapiens) and respondents

dogs (Canis lupus familiaris) and domestic cats (Felis catus) recorded during the tick season of 2008 for the different

Swedish regions

Region (two or moreprovinces, landskap)

Median, (no. obs.), maximum no.ticks per tick-infested human, and

(no. and % of uninfested humans)

Median, (no. obs.), maximum no.ticks per tick-infested dog, and

(no. and % of uninfested dogs)

Median, (no. obs.), maximumtotal no. ticks per cat, and (no.

and % of uninfested cats)Northern North:Norrbotten and Lappland

1b NS (5) 1 (95; 95.0%) 2a NS (26) 12 (5; 16.1%) 1 ab NS (34) 10 (4; 10.5%)

Central North: Medelpad andngermanland, Hrjedalen,Jmtland, Vsterbotten

1.5a NS (2) 2 (22; 91.0%) 2 a NS (11) 20 (1; 8.6%) 2 b NS (10) 8 (1; 10.0%)

Southern North: Dalarna,Gstrikland and Hlsingland

2a NS (43) 15 (35; 81.1%) 10 a ** (45) 1000 (0; 0%) 11b *** (36) 200 (1; 2.7%)

Central: Dalsland, Vrmland,Vstmanland, Nrke,Sdermanland and Uppland

5 b *** (311) 225 (58; 18.6%) 25 a *** (123) 1000 (0; 0%) 27.5c *** (156) 100 (0; 0%)

West Coast: Halland,Vstergtland and Bohusln

7b *** (163) 125 (26; 15.9%) 18a *** (54) 500 (2; 3.5%) 25bc *** (75) 1000 (1; 1.3%)

South-East, Baltic Islands:land and Gotland,

4 b *** (20) 52 (5; 20.0%) 12.5a *** (6) 120 (1; 14.2%) 20bc *** (10) 500 (0; 0%)

South: Skne, Blekinge,Smland and stergtland

5 b *** (201) 125 (46; 18.6%) 21.5a *** (86) 1500 (2; 2 .3%) 30b ***(99) 250 (1; 1.0%)

All provinces (landskap) 5*** (745) 225 (287; 27.8%) 15 (351) 1000 (11; 3.0%) 20 (420) 1000 (8; 1.8%)

Medians denoted with the same letter in a column are not significantly different at p = 0.05 (t-test of geometric means). The asterisks at the Wald c2 -values

indicate whether the corresponding geometric mean for the region is different from 0.0; ** 0.01 < P > 0.001, *** = P < 0.001, NS = not significant. In parentheses,

after the median number, is shown the number of valid observations on which the median is based, and thereafter the maximum total number of tick

specimens estimated by a respondent on one individual host. The last figures (in parentheses) in each column are the number and percentage of hosts without

any ticks.



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mainland during the last 30 years, in particular since1988 to present time.

Population dynamic aspectsIn response to climate change, populations can shift theirdistribution, adapt to the new climate or go extinct; shiftsof their distributions can be pole ward to higher latitudesor upwards to higher altitudes [41]. Theory and limitedempirical data suggest that shifts in population abun-dance along the edge of the range should be one of thefirst and most sensitive signs of a broader speciesresponse to environmental change [41]. The rangeextension ofI. ricinus in Sweden is at the northern edgeof the ticks geographical distribution. It is in such mar-ginal areas that we obtained the first indications about aresponse ofI. ricinus to the changing climate and hostabundance [14]. Here, at the limit of its range, environ-

mental conditions are, in general, less optimal. The tickpopulation will therefore be more likely to go extincthere than in its core area. Thus, it is likely that the distri-butional area ofI. ricinus in North Sweden, as presentedon the right map of Figure 3, might change: during some

years the ticks range may enlarge whereas during otherless favourable years it may retract.

Organisms are usually more abundant at the centre oftheir range, where optimal biotic and abiotic conditionsusually prevail, than towards the periphery [42]. The dataon median numbers of ticks recorded by the respondentson themselves, and on their dogs and cats suggest thatthese medians are greater in southern and centralSweden than in northernmost Sweden. This supports the

view that tick density is, in general, much lower near theperiphery of its range.

Near the core of the distributional range of I. ricinus inCentral Europe a phenomenon similar to that observedby us in North Sweden was observed: In the CzechRepublic I. ricinus extended its range to higher altitudes.Thus, ticks infected with the TBE virus (TBEV) and sev-eral species of the B. burgdorferi s.l. complex were col-lected during the last decade at higher altitudes thanbefore [20,21,43]. Tick range expansion can be facilitatedby human activity, for example when tick-infested dogs,

cattle or other domesticated mammals are brought intopreviously tick-free areas. A few such cases where it issuspected that ticks, found in previously tick-free local-ities in northern Sweden, had dropped from dogs thathad shortly before visited tick-infested areas in central orsouth Sweden were reported by informants during oursurvey (TGT Jaenson DGE Jaenson, unpublished data).However, we believe that in Sweden the main vehicle forrapid and effective transportation of ticks of all stagesinto new areas are roe deer and to a lesser extent otherlarge mammals. Birds are important transporters ofimmature I. ricinus, which may be infected with Borrelia

bacteria and other pathogens of humans [44-46]. In con-trast to some other bird-parasitizing tick species, I. rici-nu s ticks on birds are very rarely adults [44-46].Therefore, they are unlikely to establish new tick popula-tions in tick-free areas. However, such immature ticksmay introduce new pathogens into previously non-endemic areas.

Roe deer - the main host for females of Ixodes ricinusThe abundance of ticks is largely determined by the avail-ability of suitable hosts [22,23,29,30,47-49]. In many partsof Europe including Sweden, the roe deer has for the lastdecades up to the present time been the most importantblood meal host for females of I. ricinus [13,14,22,23,48]and a mate-seeking site for the tick males [13]. Conse-quently, the roe deer population is a key factor for thereproductive success of the tick population. In North

America, the white-tailed deer (Odocoileus virginianus)plays a similar role as an important host for I. scapularis[42,47,50]. In Central Sweden in the late summer, onesingle roe deer can harbour > 2000 I. ricinus ticks; Meaninfestation rates of 30 females, 17 males, 93 nymphs and265 larvae ofI. ricinus were recorded on 37 roe deer byTlleklint & Jaenson [51]. A growing number of roe deeris therefore likely to have been of major importance forthe ticks increasing abundance and range expansion fromthe 1980s.

To obtain support for the hypothesis that there is acausal link between changes in deer distribution andabundance and similar changes in tick distribution andabundance, one would need to establish if such changesindeed have coincided in space and time [24]. In GreatBritain people consider that the increases in tick numbersover recent years coincide spatially with increases in deernumbers; peoples perceptions were supported by datashowing simultaneous increases in tick infestation rateson grouse and roe deer [24].

For reasons explained earlier, the roe deer populationin Sweden expanded to very high levels during the 1980sand 1990s, reaching a peak in 1993-94. The subsequentspread of ticks northwards in Sweden were most likely aresult of the greater availability of hosts, particularly roe

deer, and a changing climate that was directly and indir-ectly favourable for both ticks and roe deer [8,14,26].Extended vegetation periods and mild winters have con-tinued in most years after the early 1990s.

On the Swedish mainland the number of roe deer hasrecently declined, partly due to increasing numbers ofpredators but more importantly due to two cold winters(2009/2010 and 2010/2011) with heavy snow cover [15].However, the roe deer has a great reproductive potentialand great dispersal capacity [16], and during winter-timemany hunters are providing fodder to increase deer sur-

vival and reproduction in order to maintain large



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numbers of deer for hunting. Therefore, if counter-mea-sures are not undertaken, to keep the roe deer andother deer populations at low, acceptable levels in linewith public health objectives, they are likely to rapidlyregain high population levels.

The geographic range of roe deer in Sweden covers alarger area than the one where I. ricinus has beenrecorded. Thus, in 1990 roe deer were only absent fromthe north-western part of Lapland in North Sweden[16]. This implies that, provided the climate will be sui-table for I. ricinus this tick may be able to establish per-manent populations in areas of North Sweden wherethe tick is still absent but where the main host for theadult stage, the roe deer occurs.

A characteristic behavioural trait of young roe deer istheir tendency to rapidly disperse to new areas, often faraway from their place of birth [16]. Nearly all young deer

in North Sweden appear to leave their place of birth [16].While young deer in South Sweden usually do not dis-perse more than 20 km from their place of birth the cor-responding mean distance in North Sweden is > 40 kmwith some of the migrations as far as 200 km [16], pre-sumably due to greater distances between favourablehabitats in North Sweden than in South Sweden. Thisbehaviour strongly supports the hypothesis that roe deerhas greatly contributed to the recent rapid and massivespread ofI. ricinus throughout northern Sweden.

What other factors are causing the increasing range andabundance of the tick and increased human incidence oftick-borne pathogens?Changes in climate and vegetation are two key factors thatwill profoundly impact both I. ricinus and its host animals.Many other factors may be regarded as additional driversthat have affected and will affect the abundance and rangeofI. ricinus in Sweden and neighbouring countries. Theseinclude increased availability of large blood hosts, espe-cially cervids, for the tick females and for both sexes touse as mating sites; migration and dispersal capacity ofwild animals, especially deer; and migration and transpor-tation of medium-sized to large domesticated mammals.Other factors are diseases affecting deer, hares and phea-

sants or their predators; changed hunting pressures ontick hosts or on their predators; provision of winter feedto deer, hares and pheasants; changed agricultural andfarming practices; changed grazing methods; changed landuse patterns; and reduced or lost diversity of tick host ani-mals and their predators in the ticks food web [40,52]including increased abundance or disappearance of verte-brates affecting the abundance or behaviour of blood hostsof ticks; importation and spread of non-native tick hostanimals; changed environmental and conservation legisla-tion and strategies; creation or establishment of protectedor recreational areas such as nature reserves, national

parks, forest reserves and urban parks; feeding of deer andother wild animals close to or in urban areas; immigrationof deer into urban areas and increased availability for ticksof deer, hares, dogs and pheasants in such areas; greaterhuman exposure to ticks due to changed leisure activitieswith more outdoor activities to promote well-being andhealth; increased berry and mushroom picking; more lei-sure time; changed/increased awareness of and greaterability to detect and remove ticks; increased awareness bydoctors and laymen of tick-borne disease symptoms andincreased testing for infection leading to increased report-ing of ticks bites and tick-borne diseases; greater aware-ness oftick high-risk areas and TBE high-risk areas;and changed incidence of TBE due to altered TBE vacci-nation rates.

Lyme borreliosis and TBE incidences in Sweden

Roe deer can be infested with Borrelia- [53] and presum-ably also with Anaplasma-, Rickettsia-, Babesia- andTBE-virus-infected I. ricinus. Therefore, roe deer arelikely to play an important role in the dispersal to newlocations of ticks infected with human pathogens. Manynew TBE-foci have been detected in Sweden duringrecent years [54-56]. The large roe deer population andthe great dispersal potential of deer [16] infested withpathogen-infected ticks, in combination with a warmerclimate with more rapid rise in late spring and early sum-mer temperature permitting simultaneous co-feeding ofinfectible tick larvae together with infected nymphs, mayhelp to explain why such new TBEV-foci have appearedfar away from the old TBEV-endemic areas. Also, therapid spread of the tick and tick-borne infections intocentral and northern Sweden is presumably mainly dueto transportation of infected ticks on migrating roedeer. It is presumably to a much lesser extent due todogs, which have visited more southern parts of Sweden,infested with Borrelia-infected ticks and northward-migrating birds infested with Borrelia- and TBEV-infected ticks [44-46].

In Sweden, the geographical distribution of human-pathogenic LB spirochaetes, B. burgdorferi s.l., coincideswith that of their main vector, I. ricinus [27-30]. In

other words, changes in tick distribution and tick den-sity are likely to have increased the risk of human LBand TBE and are likely to lead to further changes in riskareas of these and other tick-borne infections.

The highest incidence of LB reported for Europe is inEastern Central Europe, with incidence figures of 120-130human cases per 100,000 inhabitants/year recorded in Slo-

venia and Austria, respectively [57]. We found that the LBendemic area in Sweden may have a similar, high annualincidence rate: about 125 LB cases/100,000 inhabitants [7].There are significant relationships between roe deer den-sity and abundance of I. ricinus [23,29,30,58], nymphal



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abundance and density of Borrelia- infected nymphs[29,30,39] and between density of Borrelia- infectednymphs and LB incidence in humans [57]. Thus, theabundance of roe deer may be used as a crude indicator ofrisk for human exposure to LB spirochaetes. However,since roe deer are incompetent hosts for B. burgdorferi s.l.[53] they may at very high densities divert larval ticks fromfeeding on reservoir-competent hosts to feeding on deer.This will result in a negative relationship between the den-sity of I. ricinus nymphs and the density of nymphsinfected with B. burgdorferi s.l. [30]. Similar relationshipsas for LB also exist between roe deer density and tick den-sity and incidence of human TBE cases [59]. Thus, if theabundance and range of roe deer is maintained in Sweden,tick density and the tick s range are likely to increasefurther. Consequently, the incidences of human diseases

vectored by I. ricinus are likely to become even higher.

The fallow deer, Dama dama, occurs in Sweden. It is gen-erally much less abundant than the roe deer and has alower tendency to disperse compared to that of the roedeer. However, the fallow deer population is on theincrease in some localities and is likely to become anotherimportant tick host and public health problem, especiallyin periurban areas in Sweden.

ConclusionsThe results of this follow-up study suggest that I. ricinushas continued to expand its range in northern Swedenover the last 16 years where it is now present at up toabout 66N. Ixodes ricinus has also become more abun-dant in Central and Southern Sweden. Since the risk ofLyme borreliosis follows the density of I. ricinus, LB isnow an emerging risk in North Sweden. Changes in cli-mate, in particular increased duration of the vegetationperiod and milder winters, and increased abundance ofroe deer likely combined to cause the increased range andabundance of the ticks and thereby the risk of tick-bornediseases. The appearance of new TBEV foci may be theresult of transportation of TBEV-infected ticks by roe deerand other dispersing or migrating tick hosts such as birds.

The changes in climate that we are observing today aremainly due to human activities [60]. There is an accentu-

ated temperature increase in the Scandinavian mountains,in part due to the tree line advancing into higher altitudesin response to changes in climate [61]. This will increasethe potential for the tick to continue to expand its rangenorthwards in Sweden and may also lead to increasedtransmission of tick-borne pathogens [7,62]. By the end ofthis centuryI. ricinus infected with B. burgdorferi s.l. may,in suitable habitats, include most of the ScandinavianPeninsula apart from the Scandinavian mountain range[7]. Unless populations of large mammalian hosts, in parti-cular deer, of adult ticks are rigorously controlled by hunt-ing and other methods such as protection of lynx and less

intensive hunting of the red fox the ticks range and abun-dance of ticks will most likely increase further. This willpresumably lead to increased risk of human tick-borneinfections in northern Scandinavia.

Author detailsTJ and DJ: Medical Entomology Unit, Department ofSystematic Biology, Evolutionary Biology Centre,Uppsala University, Norbyvgen 18d, SE-752 36Uppsala, Sweden. LE, Department of Microbiology,Immunology and Pathology, Colorado State University,Fort Collins, CO 80526, USA. EP: Department of Ani-mal Ecology, Evolutionary Biology Centre, Uppsala Uni-

versity, SE-752 36 Uppsala, Sweden. EL: Institute ofEnvironmental Medicine, Karolinska Institutet, SE-17177 Stockholm, Sweden.

Appendix I. Questionnaire used in the 2009 studyand published in Swedish in several magazinesand newspapers in SwedenQuestionnaire from Uppsala University

Please help us to map the distribution of the tick!

Please answer the questions and send the question-

naire to the address below!

We are very grateful if you would like to answer thefollowing questionnaire.

We are equally interested in no answers as yesanswers.

We are particularly interested in data from Norrland(North Sweden) and northern Dalarna. We also want tohave any ticks from this area. Place the tick in a jar orbox in two well-tied plastic bags. Note that it is impor-tant that you fill in your address.

Send the questionnaire (and if possible any ticks) toThomas Jaenson, EBC, Uppsala University, Norbyvgen18d, 752 36 Uppsala

Are there ticks within 1 km from your home? YES____ NO_____

How many ticks did you find on you, or on your dog,or cat, near/within 1 km from your house in 2008?Please give the total number of ticks found during thewhole season per person and per animal

Dog: ______ Cat: ______ Human: ______Were there any ticks around your home in the early

1990s? YES____ NO______ Do you think that ticks around your home is less

common, about equally common or more common nowthan in the early 1990s?

Rarer now:____No change:_____

More common now: ______Any other comments of interest for tick science":Your name:________________________________Address:________________________________



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Zip Code:_________Phone number: ______________________Landskap (province):___________________

AcknowledgementsWe are very grateful to: all persons who responded to the questionnaires; toall persons who sent us ticks for identification, in particular Mrs MarlnSandstrm, Holmn, staff members of Berguvens Veterinary Clinic, Sundsvalland the District Veterinary Clinic, Hede; and to two anonymous reviewers forhelpful suggestions on the manuscript. For publishing an information paperabout ticks and the tick survey questionnaire we thank the editors of thefollowing monthly magazines and newspapers: Tidningen Apoteket (ThePharmacy), Brukshunden (The Service Dog), Vi i Villa (We Home Owners),Svensk Jakt (Swedish Hunting) and three North-Swedish newspapers(Lnstidningen stersund, Norrbottenskuriren, Pite Tidningen). For fundinghis research on ticks and tick-borne infections TJ acknowledges financialsupport from Carl Tryggers Stiftelse and Magnus Bergvalls Stiftelse.

Author details1Medical Entomology Unit, Department of Systematic Biology, EvolutionaryBiology Centre, Uppsala University, Norbyvgen 18d, SE-752 36 Uppsala,

Sweden. 2Department of Microbiology, Immunology and Pathology,Colorado State University, Fort Collins, CO 80526, USA. 3Erik Petersson,Department of Animal Ecology, Evolutionary Biology Centre, UppsalaUniversity, Norbyvgen 18d, SE-752 36 Uppsala, Sweden. 4Elisabet Lindgren,Institute of Environmental Medicine, Karolinska Institutet, SE-171 77Stockholm, Sweden.

Authors contributionsTJ designed the 2009 study, based on the 1994 study, collected andanalysed the data, reviewed the literature and wrote the initial and finalversions of the manuscript. DJ collected, compiled and co-analysed the data,wrote a computer program and co-refined the intellectual content of themanuscript. LE initiated this research by the 1994 study for which he hadthe main responsibility; LE and EL co-analysed the data and co-refined theintellectual content of the manuscript. EP co-analysed the data and carriedout the statistical analyses. All authors read and approved the final version

of the manuscript.

Competing interestsThe authors declare that they have no competing interests.

Received: 16 October 2011 Accepted: 10 January 2012

Published: 10 January 2012

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doi:10.1186/1756-3305-5-8

Cite this article as: Jaenson et al.: Changes in the geographicaldistribution and abundance of the tick Ixodes ricinus during the past 30years in Sweden. Parasites & Vectors 2012 5:8.

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